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The Pharma Innovation Journal 2019; 8(3): 22-30

ISSN (E): 2277- 7695 ISSN (P): 2349-8242 NAAS Rating: 5.03 First report on the use of gastropod shells by hermit TPI 2019; 8(3): 22-30 © 2019 TPI from the eastern coast, India www.thepharmajournal.com Received: 11-01-2019 Accepted: 15-02-2019 Samir Sardar, Debojyoty Ghosh, Pradipta Kumar Ghosh, Koustav

Samir Sardar Bhattacharjee and Koushik Pal Department of Zoology, Ramakrishna Mission Abstract Vivekananda Centenary College, The assemblage of different in the shoreline ecotone region are potential indicators for Rahara, West Bengal, India maintaining structural and functional integrity of the coastal ecosystem. The hermit crabs among the

Debojyoty Ghosh different crab species of this habitat is notable for understanding the intrinsic relationship of the crab Department of Zoology, West dependence on gastropod shells which is important to explain the shell use pattern in . Random Bengal State University, P.O. sampling of specimens was done from the of extended mud flats of Bakkhali and Malikapur, North 24 Parganas, Frazerganj of Indian Sundarban for a period of one year, which showed greater availability of one type of West Bengal, India Telescopium telescopium. Twenty one different types of gastropod shells were chosen by Clibnarius infraspinatus and Clibnarius padavensis as their microhabitat, among which later shows Pradipta Kumar Ghosh greater affinity for Telescopium shells. The statistical analysis showed that the crab weight and shell Postgraduate Department of weight are positively correlated at a significant level (p< 0.01). Present communication also suggests Zoology, Barasat Government preference of microhabitat selection by hermit crabs depends on various factors like, spatial distribution College, 10, K.N.C. Road, and availability of resources, durability of the shells, inner columellar space, coiling of shells and Barasat, North 24 Parganas, association of epibiotic covering of the shells (scallops and barnacles). West Bengal, India

Keywords: Ecotone, gastropod shells, Indian Sundarban, microhabitat selection Koustav Bhattacharjee Postgraduate Department of Zoology, Barasat Government 1. Introduction College, 10, K.N.C. Road, Sandy beaches are the dynamic environment within which crab diversity are Barasat, North 24 Parganas, maximum. Among all the crab species, the anomuran hermit crab is special for their West Bengal, India morphology and complex behavior of shell choice. Hermit crabs actively transport, recycle, [1] Koushik Pal and concentrate gastropod shells in this zone (Thompson et al., 1985) . After Department of Zoology, they opt for empty molluscan shells as their temporary refuge (microhabitat) for protecting University of Kalyani, Nadia, their soft vulnerable abdomen from erosion and predation (Vance, 1972; Angel, 2000) [2, 3], West Bengal, India desiccation (Taylor, 1981; Brodie, 1999) [4, 5] and osmotic stress (Shumway, 1978) [6]. A pioneer work on hermit crab shell selection behaviour started by Thompson (1910) [7] and

continued till present time are indicative of the enormous importance of hermit crabs shell selection behavior which varies with different habitats, acting in different ways on each crab species (Bertness, 1981) [8], in different areas (Garcia & Mantelatto, 2000) [9]. The empty molluscan shells chosen are from gastropods (Reese, 1963; Hazlett and Provenzano, 1965; Harvey and Colasurdo, 1993; Brodie, 1999) [10, 11, 12, 5] and this selection in the natural habitat

depends on various factors like availability of molluscan shells (Bollay, 1964; Reese, 1962; Vance, 1972a; Bach, Hazlett and Rittschof, 1976 and Kellog, 1976; Conover, 1978; Bertness, 1982; Pinheiro et al., 1993; Floeter et al., 2000; Turra and Leite, 2001; Sant’Anna et al., 2006) [13, 14, 15, 16, 17, 18, 19, 20, 21, 22, 23], predator presence (Rotjan et al., 2004) [24], hydrodynamics (Hahn, 1998) [25], dilution of sea water (Davenport et al., 1980) [26], chemical cues (Mesce, 1982; [27, 28] [29, Benoit et al., 1997) abrasion and extremes of temperature (Reese, 1969; Vance, 1972) 2] . In addition to these factors choices on specificity for shell types (Reese, 1962; Hazlett, 1978; Abrams 1978; Conover, 1978; Elwood, Mc. Clean and Webb, 1979; Bertness, 1980) [14, 30, 31, 18, 32, 33], crab growth rate (Wada et al., 1997) [34]; shell use history (Elwood et al., 1979; Turra [32, 35] [36] and Leite, 2003) and environmental threats (Bulinski, 2007) also makes the pattern of Correspondence shell selection a much more complicated process to understand this system. Shell species- Samir Sardar preference appears to be related to the angle of the of the shell with the substratum Department of Zoology, (ground) and the posture of the crab whilst inhabiting the shell was studied by Dowds and Ramakrishna Mission Elwood (1982) [37]. Fewer studies have investigated discrimination of gastropod shells based Vivekananda Centenary College, [18, 38, 39, 40] Rahara, West Bengal, India on shell condition (Conover 1978; McClintock 1985; Wilber 1989; 1990) . ~ 22 ~ The Pharma Innovation Journal

In this case of shell discrimination, hermit crabs use their rich foraging ground for the hermit crabs. tactile cues to judge between intact shell and drilled shell (Pechenik and Lewis 2000) [41]. A close intricate relationship 2. Materials and Methods exists between hermit crabs and its’chosen gastropod shells 2.1 Study Area which directly influence the life history stages of the hermit The field study on hermit crabs and its’sampling for specimen crabs and its’ survivality. Hence studying this microhabitat collection was done on the extended beaches of Bakkhali and selection pattern is very important to understand the close knit Fraserganj of Namkhana island located in the district of South ecology of this crab species. 24 Parganas, West Bengal, India with latitude 21034/ N and Majority of the studies on hermit crab abundance and shell longitude 88015/ E. The sampling area of the intertidal zone of use/ choice was made on the western coast of India. the beach (Fig 1) covers a minimum width of about 90 meters Unfortunately, no such study was done from the eastern coast (Fraserganj area) to a varying width of 180- 240 mt. towards of India. So an attempt was made to study the species the estuary (Bakkhali mohona). The beach was extended abundance of hermit crabs and their shell utilization pattern nearly 1 km towards Fraserganj and 2 km towards estuary from a small coastal region of Sundarban Biosphere Reserve, from the entry point of Bakkhali beach during extreme low South 24 Parganas (West Bengal, India) where the beach is tide. enormously exposed during extreme low tide, facilitating a

Fig 1: Map of the study area.

2.2 Methodology (HCHO) solution for laboratory analysis and identifications. The present work was conducted from January 2017 to Analysis on morphometry of both crabs and shells (Fig. 2) December 2017 (irrespective of seasons and months) during were done with the help of slide calipers and respective which different types of gatropod shells irrespective of size weights were taken by the help of electronic weigh balance and weight inhabited with hermit crabs (considered as chosen) (Keory 300). Taxonomic identification of gastropod shells and those shells which do not inhabit hermit crabs (considered was done following the classification of Vaught (1989) [42] as as unchosen) were randomly handpicked from the natural documented in Catalogue of marine mollusks- polyplacophora habitat of the intertidal zone of the sea shore. Specimen and (Dey2016) [43]. Further taxonomic collection was effective only at the time when the beach was identification of hermit crabs upto the possible lower extensively exposed during low tide. After the collection of taxonomic category was done following the classification samples, gastropod shells both (chosen and unchosen) were scheme of Ajmal Khan and Natarajan, R. (1984) [44] and by stored within big plastic jars containing 4% formaldehyde the help of scientists of Zoological Survey of India (ZSI),

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Kolkata. The durability of different types of gastropod shells durability of the molluscan shells and two-tailed single t-test was also tested in the laboratory by acid digestion in 3(N) was performed to analyze the result. Hydrochloric acid (HCl) at room temperature to determine the

Fig 2: Morphometric measurements of hermit crab and its shell

3. Results and Discussions Telescopium shells in abundance. But C. infraspinatus was A total of 2480 different types of gastropod shells were found to exist everywhere in the intertidal zone and their collected as samples and out of which 1230 gastropod shells distribution is much more influenced by the distribution of were unchosen. Among the rest, twenty one shell species empty gastropod shells. The shell use pattern as studied were identified. It has been observed that, only earlier in hermit crabs may vary and their coexistence may two species of hermit crabs, namely, Clibnarius padavensis attribute to shell (Grant and Ulmer, 1974; Floeter et al., 2000; (Fig 3a) and Clibnarius infraspinatus (Fig. 3b) were occupied Turra and Leite 2002; Oba et al., 2008) [46, 47, 48, 49]. Clibnarius in all the twenty one gastropod shells as their microhabitats. infraspinatus commonly known as orange striped hermit crab Alcock (1905) [45] reported these two species for the first time were moderate in number to that of Clibnarius padavensis as from India. identified during laboratory study. But juveniles were difficult These two crab species coexist in the sandy intertidal zone to identify specieswise and hence crab abundance was not where C. padavensis prefer to forage in the mud flats of analysed clearly. mohona region (upper intertidal zone) along with

(a) padavensis (b) Clibanarius infraspinatus

Fig 3: Two species of hermit crab from the Bay of Bengal (India).

Female hermit crabs were determined by the presence of good quantity of bright, berried red eggs found on the gonopores (Fig4a) ventral to the cephalothoracic-abdominal pleopods of the crab (collected during the months of junction of matured big crabs and by egg content on the September and October). But females are less abundant in the pleopods (Fig 4b). Almost all the females are gravid with muddy flats of Bakkhali beach relative to Fraserganj beach.

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4a 4b 4c

Fig 4a: Gonopores in female crab (in red circle) Fig 4b and 4c: Gravid female crabs showing location of eggs

to the remote eggs within the shell Vermeij (2012) [50]. In other studies, high intertidal hermit crabs namely obscures and Clibanarius albidigitus preferred highly spiral shells, because those shells hold more water and therefore prevent desiccation (Bertness, 1981a,b) [51, 52].

Fig 5: Male- female abundance of Hermit crabs

The gastropod shells during laboratory analysis showed that shells chosen by gravid females have less or no epibiotic coverings (barnacle colonies and scallops), but shells chosen by male crabs have more barnacle colonies and scallops ornamentation. The Telescopium shells have much elaborate ornamentations relative to other large shells. This epibionts

increases the weight of the shells which is an extra load to Fig 6: Shell opening showing secondary slits inside T. telescopium bear with hermit crabs during foraging. Male crabs opt for shell earlier inhabitated by gravid C. padavensis. shells with high epibiotic covering which may be a signal of honesty to be selected by female crabs during sexual In the present study the relative percentage of chosen selection. According to Bach et al. (1976) [16], the presence or gastropod shells by hermit crabs was 50.4 and the unchosen absence of epibionts on shells has a strong effect on the shell percentage of gastropod shells was 49.6. Among the chosen use pattern in hermit species with lower shell selectivity. shells, twenty one different types of gastropod shells were Presence of secondary slit or opening in the chosen shells selected as the hermit microhabitat (Table 1), out of which were found among all the gravid females which may be either eighteen are of marine molluscs and three species are fresh for release of eggs or may be to facilitate effective respiration water molluscan shells.

Table 1: Diversity of different gastropod shells chosen by Hermit Crabs

Serial No. Shell types Marine Molluscan Shells Codes 1 Nerita (Amphinerita) articulata Gould NB 2 Cerithidea (Cerithidea) obtusa Lamarck CO 3 Cerithidea (Cerithideopsilla) cingulated (Gmelin) PC 4 Telescopium telescopium (Linnaeus) TT 5 Polinices (Polinices) mamilla (Linnaeus) PM 6 Polinices (Neverita) didyma (Roeding) ND 7 Natica (Natica) tigrina (Roeding) NT 8 Natica (Natica) vitellus (Linnaeus) NV 9 dolium (Linnaeus) TD ~ 25 ~ The Pharma Innovation Journal

10 Gyrineum natator (Roeding) GN 11 Bufonaria rana (Linnaeus) BR 12 Thais blanfordi (Melvill) IB 13 Thais lacera (Born) IL 14 Nassarius (Niotha) stolatus (Gmelin) NS 15 Nassarius (Zeuxis) foveolatus (Dunker) NF 16 Pugilina (Hemifusus) cochlidium (Linnaeus) VC 17 Turricula javana (Linnaeus) TJ 18 Architectonica laevigata (Lamarck) AL Fresh Water Molluscan Shells 19 Bellamya bengalensis (Mueller) BB 20 Pila globosa (Swainson) PG 21 Melanoides tuberculata (Mueller) MT

Fig 7: Relative abundance of different gastropod shells showing diversity for shell choice.

Availability of the twenty one different types of molluscan Bellamya bengalensis, Pila globosa and Melanoides shells in the sandy shore of Bakkhali and Fraserganj showed tuberculata (these species are least concerned according to that Telescopium telescopium (TT) is the most abundant shell IUCN Red List of Threatened Species, 2017- 3) were found in type followed by Cerithidea cingulate (PC), Natica vitellus this marine ecotone region which were also chosen by hermit (NV), Pugilina cochlidium (VC), Thais blanfordi (IB) and crabs as their temporary refuge. These freshwater gastropod Thais lacera (IL) respectively (Fig. 7). Hermit crabs opt for shells have entered into the marine environment by Telescopium first rather than the other shells due to its rich inundations and runoff. Those crabs sometimes inhabit availability for their microhabitat and durability of the shells allochthonous shell species and water currents added those (described later). Although Cerithidea shells are highly freshwater shells into hermit habitat, also called as anomalous abundant (smaller shells escaped collection) in the mud flat habitat of the organism (Shimoyama et al., 1979; Yamaguchi, areas (mohona), their size and collumelar space is very 1983; Asakura and Kikuchi, 1984; Shimoyama, 1985) [54, 55, 56, narrow and cannot provide sufficient space as microhabitat 57]. except the juveniles. Thais shells have good columellar space The quality of the shells and its composition is another and are lighter shells chosen as microhabitat which is important determinant for shell preferences in hermit crabs moderately abundant. Big shells with large columellar space since shell health increases fitness of foraging, survivality, and light weight like Tonna dolium, Pila globosa are chosen fecundity and reproductive success of the hermits inhabiting by large size crabs whose abundance is low in the crabitat. As within it. Chemical erosions, wave actions, hydrodynamics hermit crabs actively transport, recycle, and concentrate (Hahn, 1998) [25], dilution of sea water (Davenport et al., gastropod shells in this zone (Thompson et al., 1985) [1], their 1980) [26], chemical cues (Mesce, 1982; Benoit et al., 1997) preference of choice for a specific shell type is least rather [27, 28], abrasion and extremes of temperature (Reese, 1969, shell supply by dying gastropods and other hermit crabs Vance, 1972b) [29, 58] etc. act continuously on the shells in the (Turra and Denadai, 2004) [53] regulates their occupancy for nature for delimiting its quality against selection. Hence shells. Hence the choice of shells may be under competition durability is an important criterion of the shells to be taken for the two species of hermit crabs which is site specific into consideration while studying the shell choice in hermit depending on shell availability or may be some species of crabs. So only large and heavy shells which were moderately hermit have more preference for some shell types which may to highly abundant were taken for the durability test to be innate behavior or learnt (shell use history) according to determine the rate of decay or degradation (Fig. 8). Out of Elwood et al. (1979) [32]; Turra and Leite (2003) [35]. eleven shells VC showed the high rate of degradation while In the present study only three freshwater molluscan shells MT the least. ~ 26 ~ The Pharma Innovation Journal

Fig 8: Acid digestion of selected Molluscan shells

After two-tailed single t-test, it was observed that the rate of shells (both chosen and unchosen) showed that there exists a shell digestion is varying significantly (t=2.722, df=10, p< positive correlation between crab weight (wt.) and shell 0.05) among different shell types. This indicates that different weight (r= 0.536), ie. if the crab increases in size and in shell types have different chemical compositions on which the weight, it will opt for a new shell which is more heavier and rate of digestion (ie. durability) depends. larger than the previously chosen shell. Shells like MT, PC, NS, NT etc. have very low rate of decay of shells in HCl acid; hence are much durable shells (valued Table 2: ANOVA table to determine significance between chosen shells) in comparison to others due to change in some and unchosen shells.

unknown chemical composition of the shells. Shells like VC, Shell characters F value Significance TT, ND etc. have high rate of decay; hence are poorer shells Shell length 25.893 p< 0.01 in durability test (low –valued shells). But the presence of Shell weight 17.535 p< 0.01 hermit crabs was also observed in those low valued shells Shell length 87.379 p< 0.01 irrespective of their low durability indicating that, the Shell aperture breadth 57.264 p< 0.01 availability of empty molluscan shells is low for shell choice due to unpredictability of the shell supply, a common The above ANOVA table (Table 2) showed that among the situation in nature and severe competition may exist for the chosen and unchosen gastropod shells, four shell characters choice in the two species C. padavensis and C. infraspinatus. are varying at significant level (p< 0.01). This indicates that Hence absence of preference is found in hermit crabs for four shell characters (shell length, shell weight, shell aperture choosing such a diversity of twenty one different types of length and shell aperture breadth) have important influences molluscan shells as their microhabitat. on shell selection for these intertidal hermit crabs. The morphometric study of hermit crabs and its’ molluscan

Table 3: Pearson correlation matrix between selected characters of female hermit crab and selected characters of their chosen shells

Female TCL CW CAL SL SW SAL SAB EW TCL 1 0.950** 0.837** 0.705** 0.708** 0.897** 0.910** -0.189 CW 1 0.829** 0.630** 0.652** 0.893** 0.929** -0.148 CAL 1 0.826** 0.855** 0.663** 0.787** 0.086 SL 1 0.888** 0.527** 0.648** 0.194 SW 1 0.477** 0.669** 0.117 SAL 1 0.859** -0.287* SAB 1 -0.233 EW 1 (TCL= total crab length, CW= crab weight, CAL= crab abdominal length, SL= shell length, SW= shell weight, SAL= shell aperture length, SAB=shell aperture breath, EW=egg weight).

The above correlation table (Table 3) showed that crab length breadth) are also showing high positive correlation with crab and shell length are positively correlated (p< 0.01) which wt. (p< 0.01) indicating that with the increase in crab size and indicates that with increase in body size of the hermit crabs, wt., the shell aperture criteria also increases; hence they opt they opt for larger shells with increasing in volume. Similarly for larger shells with wide openings columellar space for easy the crab wt. and shell wt. has high positive correlation (r= accessibility. 0.652, p< 0.01) which states that if crab increases in size, its’ Female hermit crabs with berried eggs showed a negative weight increases, then choice for shell wt. will also increases. correlation with crab wt. and egg wt. which indicates that, The shell aperture criteria (aperture length and aperture crabs with lower body wt. can carry eggs easily. Female

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hermit crabs also showed negative correlation with shell crabs within a single populations. However another group of aperture criterias (aperture length and breadth), indicating that workers like, Grant and Ulmer (1974) [46]; Abrams (1987) [65]; they choose small aperture shells for more tightly fitting into Gherardi (1990) [66]; Floeter et al. (2000) [47]; Turra and Leite it and to prevent slippage or unwrapping during foraging with (2002) [67]; Turra and Denadai (2004) [53]; Oba et al. (2008) its’ eggs. [48]studied the shell selections in between sympatric species, where they have shown the shell selection by hermit crab is Table 4: Pearson correlation matrix between selected characters of highly plastic. male hermit crabs and selected characters of their chosen shells. Their best shell choice (optimal fit) as a microhabitat depend

Male TCL CAL SL SW SAL SAB primarily on the quality of the shell and on characters like TCL 1 0.826** 0.717** 0.634** 0.739** 0.607** shell weight, shell length, shell aperture size, inner collumelar CAL 1 0.795** 0.716** 0.471** 0.577** space, durability etc. The shell weight is the load that the SL 1 0.819** 0.489** 0.615** crabs carry along with them after their hatching from the egg SW 1 0.462** 0.596** (juvenile) and continue till death. So the crab will opt for low SAL 1 0.611** weight, high durable shell providing good efficiency to carry SAB 1 the load so that shell acquired enhances fitness, increase (TCL= total crab length, CW= crab weight, CAL= crab abdominal survival and fecundity. Ornamentations like epibiotic shell length, SL= shell length, SW= shell weight, SAL= shell aperture covering and secondary slit/ opening are also the criteria for length, SAB=shell aperture breath, EW=egg weight). shell choice behaviour. But to understand the nature of shell ** indicates values that are 99% correlated selection in hermit crabs, not a single method of *indicates values that are 95% correlated experimentation is sufficient. Hence the present study has

only explained the nature of gastropod shell use in the natural Male hermit crabs showed all crab characters to be positively habitat rather than shell selection. correlated (Table 4) with the shell characters (p< 0.01)

indicating that male crabs not only choose optimal shell 5. Acknowledgements criterias but also carry excess load bearing epibiotic coverings Authors like to express their thanks and regards to the in contrast to female choice for shells. These male specific executive committee of Social Environmental and Biological criteria of shell choice may have an important role in sexual Association (SEBA), Kolkata for their financial help in this selection in the hermit crab population which needs to be communication. Authors also like to express their special observed in the nature for detail analysis. thanks of gratitude to Principal Maharaj Swami

Kamalasthananda and Controller of Examinations, Swami 4. Conclusions Vedanuragananda Maharaj of Ramakrishna Mission The present study was an attempt to get an idea on the Vivekananda Centenery College for extending their all gastropod shell utilization pattern by two species of hermit support to complete the project. Authors are also thankful to crabs (Clibnarius padavensis and Clibnarius infraspinatus) the scientists of Crustacea and section, Zoological from their natural habitat which is highly complicated. Survey of India, Kolkata for their kind cooperation in Various factors are responsible for the shell choice behaviours identification of species. Lastly a part of the of hermit crabs which are multi-dimensional in nature. Shell acknowledgement also goes to Dr. Arunava Mukherjee, Dept use pattern in the natural habitat of Bay of Bengal is of Zoology, RKMVC College, Rahara for his help in the dependent on a combination of both site specific features preparation of the manuscript. (shell availability, silt deposition, beach exposure as foraging

ground, wave action, predators, habitat complexity and shell 6. References use history) and preference of the crab species for shells. C. 1. Thompson JB, Mullins H, Newton C. Alternative padavensis comparatively slender hermit crabs to that of C. biofacies model for dysaerobic communities. Lethaia infraspinatus, prefer to choose narrow columellar spaced, 1985; 18:167-179. highly coiled shells like Telescopium telescopium, Cerithidea 2. Vance RR. The role of shell adequacy in behavioral cingulate etc. and are found in abundant quantity on the interactions involving hermit crabs. Ecology. 1972; Bakkhali mohona beach where the shore area is muddy due to 53:1075-1083. siltation brought down from the back-water flow of the 3. Angel JE. Effects of shell fit on the biology of hermit adjacent mangrove forest areas. But the other orange striped crab longicarpus (Say). Journal of Experimental hermit crab C. pad avensis are found to forage from the upper Marine Biology and Ecology. 2000; 243:169-184. intertidal zone to the extreme lower intertidal zone of the 4. Taylor PR. Hermit crab fitness: the effect of shell sandy shore (almost 1.5 km. exposed intertidal zone) which condition and behavioral adaptations on environmental were found to inhabit within large columellar spaces of large resistance. Journal of Experimental Marine Biology and shells like Tonna dolium, Pugilina cochlidium, Thais lacera Ecology. 1981; 52(2-3):205- 218. etc. Thus both species selectivity for gastropod shells (innate 5. Brodie RJ. Ontogeny of shell-related behaviours and shell preference or learnt behavior for optimal shell, valued transition to land in the terrestrial hermit crab shell choice from shell use history) and site specific selection compressus H. Milne Edwards. Journal of Experimental (abundance of twenty one types of gastropod shells and Marine Biology and Ecology. 1999; 241:67-80. richness of a specific type of shell in a particular area) exists 6. Shumway SE. Osmotic balance and respiration in the in the study area. hermit crab, , exposed to fluctuating Several workers like, Elwood et al. (1979) [32]; Borjesson and salinities. Journal of Marine Biological Association. Szelistowski (1989) [59]; Liszka and Underwood (1990) [60]; 1978; 58:869-876. Yoshino et al. (1999) [61]; Meireles and Mantelatto (2005) [62]; 7. Thompson DAW. Historia Animalium (English Sato and Jensen (2005) [63]; Bulinski (2007) [36]; Meireles et Translaion). In: Smith JA and Ross WD (Editors) al. (2008) [64] have studied the shell selection pattern in hermit ~ 28 ~ The Pharma Innovation Journal

TheWorks of Aristotle. Clarendon Press, Oxford. 1910; shell selection behavior? Behavioral Ecology and 4:486-633. Sociobiology. 2004; 56(2):171-176. 8. Bertness M. Predation, physical stress and the 25. Hahn DR. Hermit crab shell use patterns: response to organization of a tropical hermit crab community. previous shell experience and to water flow. Journal of Ecology. 1981a; 62:411-425. Experimental Marine Biology and Ecology. 1998; 9. Garcia RB, Mantelatto FLM. Shell selection by the 228(1):35-51. tropical hermit crab Calcinus tibicen (Herbst, 1791) 26. Davenport J, Busschots PM, Cawthore DF. The influence (, Diogenida) from Southern Brazil. Journal of of salinity on behavior and oxygen uptake of the hermit Experimental Marine Biology and Ecology. 2000; crab Pagurus bernhardus (L). Journal of Marine 265(1):1-14. Biological Association UK. 1980; 60:127-134. 10. Reese ES. The behavioral mechanisms underlying shell 27. Mesce KA. Calcium-Bearing Objects Elicit Shell selection by hermit crabs. Behaviour. 1963; 21(1-2):78- Selection Behavior in a Hermit Crab. Science. 1982; 126. 215(4535):993-995. 11. Hazlett BA, Provenzano Jr. AJ. Development of behavior 28. Benoit MD, Peeke HVS, Chang ES. Use of chemical in laboratory reared hermit crabs. Marine Science cues for shell preference by the hermit crab, Pagurus Bulletin. 1965; 15:616-633. samuelis. Mar. Freshw. Behav. Physiol. 1997; 30(1):45- 12. Harvey AW, Colasurdo EA. Effects of shell and food 54. availability on metamorphosis in the hermit crabs 29. Reese E. Behavioral adaptations of intertidal hermit Pagurus hirsutiusculus (Dana) and Pagurus crabs. American Zoologist. 1969; 9:343-355. granosimanus (Stimpson). Journal of Experimental 30. Hazlett BA. Shell exchanges in hermit crabs: aggression, Marine Biology and Ecology. 1993; 165:237-249. negotiation or both. Behaviour. 1978; 26:1278- 13. Bollay M. Distribution and utilization of gastropod shells 1279. by the hermit crabs , Pagurus 31. Abrams P. Shell selection and utilization in a terrestrial granosimanus and Pagurus hirsutiusculus, at Pacific hermit crab, Coenobita compressus (H. Milne Edwards). Grove CA. Veliger. 1964; 6:71-76. Oecologia. 1978; 34(2):239-253. 14. Reese ES. Shell selection behavior of hermit crabs. 32. Elwood R, Mc. Clean A, Webb L. The development of Animal Behaviour. 1962; 10(3-4):347-360. shell preferences by the hermit crab, Pagurus 15. Vance RR. Competition and mechanism of co-existence bernhardus. Animal Behaviour. 1979; 27:940-946. in three sympatric species of intertidal hermit crabs. 33. Bertness MD. Shell preference and utilization patterns in Ecology. 1972a; 53:1062-1074. littoral hermit crabs of the Bay of Panama. Journal of 16. Bach C, Hazlett B, Rittschof D. Effects of Interspecific Experimental Marine Biology and Ecology. 1980; Competition on Fitness of the Hermit Crab Clibanarius 48(1):1-16. tricolor. Ecology. 1976; 57:579-586. 34. Wada S, Ohmori H, Goshima S, Nakao S. Shell size 17. Kellogg CW. Gastropod shells: a potentially limiting preference of hermit crabs depends on their growth rate. resource for hermit crabs. Journal of Experimental Animal Behaviour. 1997; 54:1-8 Marine Biology and Ecology. 1976; 22:101-111. 35. Turra A, Leite FPP. The molding hypothesis: linking 18. Conover Michael R. The importance of various shell shell use with hermit crab growth, morphology and shell- characteristics to the shell-selection behavior of hermit species selection. Marine Ecology Progress Series. 2003; crabs. Journal of Experimental Marine Biology and 265:155-163. Ecology. 1978; 32(3):131-142. 36. Bulinski KV. Shell-selection behavior of the hermit crab 19. Bertness M. Shell utilization, predation pressure and Pagurus granosimanus in relation to isolation, thermal stress in Panamanian hermit crabs: An competition, and predation. Journal of Shellfish interoceanic comparison. Journal of Experimental Marine Research. 2007; 26(1):233-239. Biology and Ecology. 1982; 64(2):159-187. 37. Dowds BM, Elwood R. Shell wars: Assessment strategies 20. Pinheiro MAA, Fransozo A, Negreiros-Fransozo ML. and the timing of decisions in hermit crab shell fights. Seleção e relação com aconcha emIsochelessawayai Behaviour. 1982; 85(1):1-24. Forest & Saint Laurent, 1967 (Crustacea, Anomura, 38. McClintock ST. Effects of shell condition and size upon ). Braz. Arch. Biol. Technol. 1993; 36(4):745- the shell choice behaviour of a hermit crab. Journal of 752. Experimental Marine Biology and Ecology. 1985; 21. Floeter SR, Nalesso RC, Rodrigues MMP, Turra A. 88(3):271-285. Patterns of shell utilization and selection in two 39. Wilber Jr. TP. Associations between gastropod shell sympatric hermit crabs (Anomura: Diogenidae) in south- characteristics and egg production in the hermit crab eastern Brazil. Journal of Marine Biological Association Pagurus longicarpus. Oecologia. 1989; 81:6-15. UK. 2000; 80(6):1053-1059. 40. Wilber Jr. TP. Influence of size, species and damage on 22. Turra A, Leite FPP. Shell utilization patterns of a tropical shell selection by the hermit crab Pagurus longicarpus. rocky intertidal hermit crab assemblage: I. The case of Marine Biology. 1990; 104(1):31-39. Grande Beach. J Crustac. Biol. 2001; 21(2):393-406. 41. Pechenik JA, Lewis S. Avoidance of drilled gastropod 23. Sant'Anna BS, Zangrande CM, Reigada ALD, Pinheiro shells by the hermit crab Pagurus longicarpus at Nahant, MAA. Shell utilization pattern of the hermit crab Massachusetts. Journal of Experimental Marine Biology Clibanarius vittatus (Crustacea, Anomura) in an estuary and Ecology. 2000; 253:17-32. at São Vicente, State of São Paulo, Brazil. Iheringia, Sér. 42. Vaught KC. A classification of living Mollusca. Zool. 2006; 96(2):261-266. American Malacologists Inc. Melbourne, Florida USA, 24. Rotjan RD, Blum J, Lewis SM. Shell choice in Pagurus 1989, 1-189. longicarpus hermit crabs: does predation threat influence 43. Dey A. Catalogue of Marine Molluscs (Polyplacophora

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and Gastropoda). Zoological Survey of India, 2016, 1- determine preferences for gastropod shells by a hermit- 687. crab. Journal of Experimental Marine Biology and 44. Ajmal Khan S, Natarajan R. Hermit crabs of Proto Novo Ecology. 1990; 137(1):47-62. coast. Records of the Zoological Survey of India, 61. Yoshino K, Goshima S, Nakao S. The interaction Occasional Paper. 1984; 67:25. between shell size and shell species preferences of the 45. Alcock A. Catalogue of the Indian decapod Crustacea in hermit crab Pagurus filholi. Benthos Res. 1999; 54(1):37- the collections of the Indian Museum. Anomura. Fasc. I. 44. Pagurides. Indian Museum, Calcutta, 1905, 2:1-197. 62. Meireles AL, Mantelatto FL. Shell use by the Pagurus 46. Grant WC, Ulmer K. Shell Selection and Aggressive brevidactylus (Anomura, ): A comparison Behavior in Two Sympatric Species of Hermit Crabs. between laboratory and field conditions. Acta Zoologica Biological Bulletin 1974; 146(1):32-43. Sinica. 2005; 51(5):813-820. 47. Floeter SR, Nalesso RC, Rodrigues MMP, Turra A. 63. Sato M, Jensen GC. Shell selection by hermit crab, Patterns of shell utilization and selection in two Pagurus hartae (Mclaughlin & Jensen, 1996) (, sympatric hermit crabs (Anomura: Diogenidae) in south- Anomura). Crustaceana. 2005; 78:755-760. eastern Brazil. Journal of Marine Biological Association 64. Meireles AL, Biagi R, Mantelatto FL. Influence of prior UK. 2000; 80(6):1053-1059. experience on shell selection by the white spot wrist 48. Turra A, Leite FPP. Shell utilization patterns of a tropical hermit crabs Paguru scriniticornis (Crustacea:Paguridae). intertidal hermit crab assemblage. Journal of Marine Hydrobiologia. 2008; 605:259-263. Biological Association. 2002; 82(1):97-107. 65. Abrams PA. Resource partitioning and competition for 49. Oba T, Wada S, Goshima S. Shell partitioning of two shells between intertidal hermit crabs on the outer coast sympatric hermit crabs, Pagurus middendorffii and P. of Washington. Oecologia. 1987; 72(2):248-258. brachiomastus, in north-eastern Hokkaido, Japan. Journal 66. Gherardi F. Competition and coexistence in two of the Marine Biological Association of the UK. 2008; Mediterranean hermit crabs, Calcinus ornatus (Roux) and 88(01):103-109. (Latreille) (Decapoda, Anomura). 50. Vermeij GJ. Evolution: Remodeling Hermit Shelters. Journal of Experimental Marine Biology and Ecology. Current biology. 2012; 22(20):882-884. 1990; 143(3):221-238. 51. Bertness M. Predation, physical stress and the 67. Turra A, Leite FPP. Shell utilization patterns of a tropical organization of a tropical hermit crab community. intertidal hermit crab assemblage. Journal of Marine Ecology. 1981a; 62:411-425. Biological Association UK. 2002; 82:97-107. 52. Bertness M. Conflicting advantage in resource utilization: The hermit crab housing dilemma. The American Naturalist. 1981b; 118:432-437. 53. Turra A, Denadai MR. Interference and exploitation components in interspecific competition between sympatric intertidal hermit crabs. Journal of Experimental Marine Biology and Ecology. 2004; 310(2):183-193. 54. Shimoyama S, Yosida T, Shuto T. Modification of paleontological information caused by selective utilization of empty shells by an intertidal hermit crab, edwardsi (Detaan). Report of the Fishery Research Laboratory. Kyushu University. 1979; 4:65-78. 55. Yajima T, Yamaguchi M. Ecological distribution of the intertidal hermit crabs and their shell utilization in the Tsukumo Bay, Noto Peninsula. Bull. Japan Sea Res.Inst. Kanazawa University. 1983; 15:1-14. 56. Asakura A, Kikuchi T. Population ecology of the sand dwelling hermit crab, Diogenes nitidimanus Terao: 1 Shell utilization. Amakusa Marine Biological Laboratory. 1984; 7:95-108. 57. Shimoyama S. Size-frequency distribution of living populations and dead shell assemblages in a marine intertidal land snail, Umbonium (Suchium) moniliferum (Lamarck), and their palaeoecological significance. Paleogeography, Palaeoclimatology, Palaeoecology. 1985; 49(3-4):327-353. 58. Vance RR. The role of shell adequacy in behavioral interactions involving hermit crabs. Ecology. 1972b; 53:1075-1083. 59. Borjesson DL, Szelistowski WA. Shell selection, utilization and predation in the hermit crab Clibanarius panamensis Stimpson in a tropical mangrove Ecology. Journal of Experimental Marine Biology and Ecology 1989; 133(3):213-228. 60. Liszka D, Underwood AJ. An experimental design to

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